{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T02:24:38Z","timestamp":1787019878831,"version":"build-2736575974"},"reference-count":37,"publisher":"Springer Science and Business Media LLC","issue":"1","content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Parasites Vectors"],"published-print":{"date-parts":[[2011,12]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>\n                      <jats:italic>Giardia duodenalis<\/jats:italic>\n                      and\n                      <jats:italic>Entamoeba<\/jats:italic>\n                      spp. are among the most common intestinal human protozoan parasites worldwide and they are frequently reported in captive non-human primates (NHP). From a public health point of view, infected animals in zoos constitute a risk for animal caretakers and visitors. In this study we carried out the molecular identification of\n                      <jats:italic>G. duodenalis<\/jats:italic>\n                      and\n                      <jats:italic>Entamoeba<\/jats:italic>\n                      spp. from nine species of primates housed in the zoological garden of Rome, to better ascertain their occurrence and zoonotic potential.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      <jats:italic>G. duodenalis<\/jats:italic>\n                      was found only in\n                      <jats:italic>Lemur catta<\/jats:italic>\n                      (47.0%).\n                      <jats:italic>Entamoeba<\/jats:italic>\n                      spp. were detected in all species studied, with the exception of\n                      <jats:italic>Eulemur macaco<\/jats:italic>\n                      and\n                      <jats:italic>Varecia rubra<\/jats:italic>\n                      . The number of positive pools ranged from 5.9% in\n                      <jats:italic>L. catta<\/jats:italic>\n                      to 81.2% in\n                      <jats:italic>Mandrillus sphinx;<\/jats:italic>\n                      in\n                      <jats:italic>Pan troglodytes<\/jats:italic>\n                      the observed prevalence was 53.6%. A mixed\n                      <jats:italic>Entamoeba<\/jats:italic>\n                      -\n                      <jats:italic>Giardia<\/jats:italic>\n                      infection was recorded only in one sample of\n                      <jats:italic>L. catta<\/jats:italic>\n                      . All\n                      <jats:italic>G. duodenalis<\/jats:italic>\n                      isolates belonged to the zoonotic assemblage B, sub assemblage BIV. Three\n                      <jats:italic>Entamoeba<\/jats:italic>\n                      species were identified:\n                      <jats:italic>E. hartmanni<\/jats:italic>\n                      ,\n                      <jats:italic>E. coli<\/jats:italic>\n                      and\n                      <jats:italic>E. dispar<\/jats:italic>\n                      .\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>Our results highlight the importance of regularly testing animals kept in zoos for the diagnosis of zoonotic parasites, in order to evaluate their pathogenic role in the housed animals and the zoonotic risk linked to their presence. A quick detection of the arrival of pathogens into the enclosures could also be a prerequisite to limit their spread into the structure via the introduction of specific control strategies. The need for molecular identification of some parasite species\/genotype in order to better define the zoonotic risk is also highlighted.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1186\/1756-3305-4-199","type":"journal-article","created":{"date-parts":[[2011,10,12]],"date-time":"2011-10-12T02:30:54Z","timestamp":1318386654000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":54,"title":["Giardia duodenalis assemblages and Entamoeba species infecting non-human primates in an Italian zoological garden: zoonotic potential and management traits"],"prefix":"10.1186","volume":"4","author":[{"given":"Federica","family":"Berrilli","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cristina","family":"Prisco","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Klaus G","family":"Friedrich","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pilar","family":"Di Cerbo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David","family":"Di Cave","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Claudio","family":"De Liberato","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2011,10,12]]},"reference":[{"key":"451_CR1","doi-asserted-by":"publisher","first-page":"195","DOI":"10.1016\/S0304-4017(98)00143-5","volume":"78","author":"E Munene","year":"1998","unstructured":"Munene E, Otsyula M, Mbaabu DAN, Mutahi WT, Muriuki SMK, Muchemi GM: Helminth and protozoan gastrointestinal tract parasites in captive and wild-trapped African non-human primates. Vet Parasitol. 1998, 78: 195-201.","journal-title":"Vet Parasitol"},{"key":"451_CR2","doi-asserted-by":"publisher","first-page":"236","DOI":"10.1016\/j.vetpar.2007.06.020","volume":"148","author":"B Levecke","year":"2007","unstructured":"Levecke B, Dorny P, Geurden T, Vercammen F, Vercruysse J: Gastrointestinal protozoa in non-human primates of four zoological gardens in Belgium. Vet Parasitol. 2007, 148: 236-246.","journal-title":"Vet Parasitol"},{"key":"451_CR3","doi-asserted-by":"publisher","first-page":"302","DOI":"10.1016\/j.vetpar.2008.05.023","volume":"156","author":"G P\u00e9rez Cord\u00f2n","year":"2008","unstructured":"P\u00e9rez Cord\u00f2n G, Hitos Prados A, Romero D, S\u00e0nchez Moreno M, Pontes A, Osuna A, Rosales MJ: Intestinal parasitism in the animals of the zoological garden \"Pe\u00f1a Escrita\" (Almu\u00f1ecar, Spain). Vet Parasitol. 2008, 156: 302-309.","journal-title":"Vet Parasitol"},{"key":"451_CR4","doi-asserted-by":"publisher","first-page":"713","DOI":"10.1128\/CMR.16.4.713-729.2003","volume":"16","author":"M Tanyuksel","year":"2003","unstructured":"Tanyuksel M, Petri WA: Laboratory diagnosis of amebiasis. Clin Microbiol Rev. 2003, 16: 713-729.","journal-title":"Clin Microbiol Rev"},{"key":"451_CR5","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1016\/S0065-308X(04)58002-8","volume":"58","author":"RCA Thompson","year":"2004","unstructured":"Thompson RCA, Monis PT: Variation in Giardia: implications for taxonomy and epidemiology. Adv Parasitol. 2004, 58: 69-137.","journal-title":"Adv Parasitol"},{"key":"451_CR6","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1016\/0020-7519(94)E0059-V","volume":"25","author":"PJ O'Donoghue","year":"1995","unstructured":"O'Donoghue PJ: Cryptosporidium and cryptosporidiosis in man and animal. Int J Parasitol. 1995, 25: 139-195.","journal-title":"Int J Parasitol"},{"key":"451_CR7","doi-asserted-by":"publisher","first-page":"1259","DOI":"10.1016\/S0020-7519(00)00127-2","volume":"30","author":"RCA Thompson","year":"2000","unstructured":"Thompson RCA: Giardiasis as a re-emerging infectious disease and its zoonotic potential. Int J Parasitol. 2000, 30: 1259-1267.","journal-title":"Int J Parasitol"},{"key":"451_CR8","doi-asserted-by":"publisher","first-page":"479","DOI":"10.1097\/00001432-200310000-00016","volume":"16","author":"W Stauffer","year":"2003","unstructured":"Stauffer W, Ravdin IJ: Entamoeba histolytica: an update. Cur Opin Infect Dis. 2003, 16: 479-485.","journal-title":"Cur Opin Infect Dis"},{"key":"451_CR9","first-page":"42","volume":"40","author":"RA Miller","year":"1990","unstructured":"Miller RA, Brondson MA, Kuller L, Morton WR: Clinical and parasitologic aspects of cryptosporidiosis in nonhuman primates. Lab Anim Sci. 1990, 40: 42-46.","journal-title":"Lab Anim Sci"},{"key":"451_CR10","first-page":"235","volume":"44","author":"HJ Hamlen","year":"1994","unstructured":"Hamlen HJ, Lawrence JM: Giardiasis in laboratory-housed squirrel monkeys: a retrospective study. Lab Anim Sci. 1994, 44: 235-239.","journal-title":"Lab Anim Sci"},{"key":"451_CR11","first-page":"116","volume":"46","author":"J Kalishman","year":"1996","unstructured":"Kalishman J, Paul-Murphy J, Scheffer J, Thomson JA: Survey of Cryptosporidium and Giardia spp. in a captive population of common marmosets. Lab Anim Sci. 1996, 46: 116-119.","journal-title":"Lab Anim Sci"},{"key":"451_CR12","doi-asserted-by":"publisher","first-page":"1089","DOI":"10.1002\/ajp.20309","volume":"68","author":"SK Vitazkova","year":"2006","unstructured":"Vitazkova SK, Wade SE: Parasites of free-ranging black howler monkeys (Alouatta pigra) from Belize and Mexico. Am J Primatol. 2006, 68: 1089-1097.","journal-title":"Am J Primatol"},{"key":"451_CR13","doi-asserted-by":"publisher","first-page":"1595","DOI":"10.1016\/j.ijpara.2009.05.013","volume":"39","author":"B Levecke","year":"2009","unstructured":"Levecke B, Geldhof P, Claerebout E, Dorny P, Vercammen F, Cacci\u00f2 SM, Vercruysse J, Geurden T: Molecular characterization of Giardia duodenalis in captive non-human primates reveals mixed assemblages A and B infections and novel polymorphisms. Int J Parasitol. 2009, 39: 1595-1601.","journal-title":"Int J Parasitol"},{"key":"451_CR14","doi-asserted-by":"publisher","first-page":"2988","DOI":"10.1128\/JCM.00013-10","volume":"48","author":"B Levecke","year":"2010","unstructured":"Levecke B, Dressen L, Dorny P, Verweij JJ, Vercammen F, Casaert S, Vecruysse J, Geldhof P: Molecular identification of Entamoeba spp. in captive nonhuman primates. J Clin Microbiol. 2010, 48: 2988-2990.","journal-title":"J Clin Microbiol"},{"key":"451_CR15","volume-title":"Book of Abstracts of the 5th Scientific Meeting of the European Association of Zoo- and Wildlife Veterinarians, Ebeltoft, Denmark, 19-23","author":"K Matz-Rensing","year":"2004","unstructured":"Matz-Rensing K, Floto A, Kaup FJ, Schaller K: Gastric amebiasis due to Entamoeba histolytica infection in a mandrill (Mandrillus sphinx). Book of Abstracts of the 5th Scientific Meeting of the European Association of Zoo- and Wildlife Veterinarians, Ebeltoft, Denmark, 19-23. 2004, May"},{"key":"451_CR16","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1007\/s10329-009-0174-x","volume":"51","author":"WL Rivera","year":"2010","unstructured":"Rivera WL, Yason JADL, Adao DEV: Entamoeba histolytica and E. dispar infections in captive macaques (Macaca fascicularis) in the Philippines. Primates. 2010, 51: 69-74.","journal-title":"Primates"},{"key":"451_CR17","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1016\/j.molbiopara.2007.02.006","volume":"153","author":"H Tachibana","year":"2007","unstructured":"Tachibana H, Yanagi T, Pandey K, Cheng XJ, Kobayashi S, Sherchand JB, Kanbara H: An Entamoeba sp. strain isolated from rhesus monkey is virulent but genetically different from Entamoeba histolytica. Mol Biochem Parasitol. 2007, 153: 107-114.","journal-title":"Mol Biochem Parasitol"},{"key":"451_CR18","doi-asserted-by":"publisher","first-page":"585","DOI":"10.1007\/s004360050169","volume":"82","author":"WL Rivera","year":"1996","unstructured":"Rivera WL, Tachibana H, Silva-Tahat MRA, Uemura H, Kanbara H: Differentiation of Entamoeba histolytica and E. dispar DNA from cysts present in stool specimens by polymerase chain reaction: its field application in the Philippines. Parasitol Res. 1996, 82: 585-589.","journal-title":"Parasitol Res"},{"key":"451_CR19","doi-asserted-by":"crossref","first-page":"916","DOI":"10.4269\/ajtmh.1998.59.916","volume":"59","author":"WL Rivera","year":"1998","unstructured":"Rivera WL, Tachibana H, Kanbara H: Field study on the distribution of Entamoeba histolytica and Entamoeba dispar in the northern Philippines as detected by the polymerase chain reaction. Am J Trop Med Hyg. 1998, 59: 916-921.","journal-title":"Am J Trop Med Hyg"},{"key":"451_CR20","doi-asserted-by":"publisher","first-page":"537","DOI":"10.1007\/s004360000205","volume":"86","author":"H Tachibana","year":"2000","unstructured":"Tachibana H, Cheng XJ, Kobayashi S, Fujita Y, Udono T: Entamoeba dispar, but not E. histolytica, detected in a colony of chimpanzees in Japan. Parasitol Res. 2000, 86: 537-541.","journal-title":"Parasitol Res"},{"key":"451_CR21","doi-asserted-by":"publisher","first-page":"255","DOI":"10.1007\/s00436-005-1415-6","volume":"97","author":"J Takano","year":"2005","unstructured":"Takano J, Narita T, Tachibana H, Shimizu T, Komatsubara H, Terao H, Kujimoto K: Entamoeba histolytica and Entamoeba dispar infections in cynomolgus monkeys imported into Japan for research. Parasitol Res. 2005, 97: 255-257.","journal-title":"Parasitol Res"},{"key":"451_CR22","first-page":"326","volume":"8","author":"LS Ritchie","year":"1948","unstructured":"Ritchie LS: An ether sedimentation technique for routine stool examination. Bull US Army Med Dep. 1948, 8: 326-","journal-title":"Bull US Army Med Dep"},{"key":"451_CR23","doi-asserted-by":"crossref","first-page":"852","DOI":"10.1128\/jcm.10.6.852-853.1979","volume":"10","author":"KH Young","year":"1979","unstructured":"Young KH, Bullock SL, Melvin DM, Spruill CL: Ethyl acetate as a substitute for diethyl ether in the formalin-ether sedimentation technique. J Clin Microbiol. 1979, 10: 852-853.","journal-title":"J Clin Microbiol"},{"key":"451_CR24","doi-asserted-by":"publisher","first-page":"44","DOI":"10.2307\/3284315","volume":"83","author":"RM Hopkins","year":"1997","unstructured":"Hopkins RM, Meloni BP, Groth DM, Wetherall JD, Reynoldson JA, Thompson RC: Ribosomal RNA sequencing reveals differences between the genotypes of Giardia isolates recovered from humans and dogs living in the same locality. J Parasitol. 1997, 83: 44-51.","journal-title":"J Parasitol"},{"key":"451_CR25","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1016\/S0020-7519(01)00340-X","volume":"32","author":"C Read","year":"2002","unstructured":"Read C, Walters J, Robertson ID, Thompson RC: Correlation between genotype of Giardia duodenalis and diarrhoea. Int J Parasitol. 2002, 32: 229-231.","journal-title":"Int J Parasitol"},{"key":"451_CR26","doi-asserted-by":"publisher","first-page":"883","DOI":"10.1007\/s00436-010-1728-y","volume":"106","author":"HL Santos","year":"2010","unstructured":"Santos HL, Bandea R, Martins LA, de Macedo HW, Peralta RH, Peralta JM, Ndubuisi MI, da Silva AJ: Differential identification of Entamoeba spp. based on the analysis of 18S rRNA. Parasitol Res. 2010, 106: 883-888.","journal-title":"Parasitol Res"},{"key":"451_CR27","doi-asserted-by":"publisher","first-page":"1444","DOI":"10.3201\/eid0911.030084","volume":"9","author":"IM Sulaiman","year":"2003","unstructured":"Sulaiman IM, Fayer R, Bern C, Gilman RH, Trout JM, Schantz PM, Das P, Lal AA, Xiao L: Triose phosphate isomerase gene characterization and potential zoonotic transmission of Giardia duodenalis. Emerg Infect Dis. 2003, 9: 1444-1452.","journal-title":"Emerg Infect Dis"},{"key":"451_CR28","doi-asserted-by":"publisher","first-page":"125","DOI":"10.1016\/j.meegid.2004.02.001","volume":"4","author":"CM Read","year":"2004","unstructured":"Read CM, Monis PT, Thompson RC: Discrimination of all genotypes of Giardia duodenalis at the glutamate dehydrogenase locus using PCR-RFLP. Infect Genet Evol. 2004, 4: 125-130.","journal-title":"Infect Genet Evol"},{"key":"451_CR29","doi-asserted-by":"publisher","first-page":"175","DOI":"10.1002\/ajp.20482","volume":"70","author":"LM Villers","year":"2008","unstructured":"Villers LM, Jang SS, Lent CL, Lewin-Koh S, Norosoarinaivo J: Survey and comparison of major intestinal flora in captive and wild ring-tailed lemur (Lemur catta) populations. Am J Primatol. 2008, 70: 175-184.","journal-title":"Am J Primatol"},{"key":"451_CR30","doi-asserted-by":"publisher","first-page":"40","DOI":"10.1016\/j.vetpar.2010.09.026","volume":"185","author":"R Beck","year":"2011","unstructured":"Beck R, Sprong H, Bata I, Lucinger S, Pozio E, Cacci\u00f2 SM: Prevalence and molecular typing of Giardia spp. in captive mammals at the zoo of Zagreb, Croatia. Vet Parasitol. 2011, 185: 40-46.","journal-title":"Vet Parasitol"},{"key":"451_CR31","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1016\/j.vetpar.2007.07.015","volume":"149","author":"HV Smith","year":"2007","unstructured":"Smith HV, Cacci\u00f2 SM, Cook N, Nichols RAB, Tait A: Cryptosporidium and Giardia as foodborne zoonoses. Vet Parasitol. 2007, 149: 29-40.","journal-title":"Vet Parasitol"},{"key":"451_CR32","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1016\/j.molbiopara.2008.04.006","volume":"160","author":"SM Cacci\u00f2","year":"2008","unstructured":"Cacci\u00f2 SM, Ryan U: Molecular epidemiology of giardiosis. Mol Biochem Parasitol. 2008, 160: 75-80.","journal-title":"Mol Biochem Parasitol"},{"key":"451_CR33","doi-asserted-by":"publisher","first-page":"1523","DOI":"10.1016\/j.ijpara.2008.04.008","volume":"38","author":"SM Cacci\u00f2","year":"2008","unstructured":"Cacci\u00f2 SM, Beck R, Lalle M, Marinculic A, Pozio E: Multilocus genotyping of Giardia duodenalis reveals striking differences between assemblages A and B. Int J Parasitol. 2008, 38: 1523-1531.","journal-title":"Int J Parasitol"},{"key":"451_CR34","doi-asserted-by":"publisher","first-page":"905","DOI":"10.1645\/0022-3395(2002)088[0905:AGDGAA]2.0.CO;2","volume":"88","author":"TK Graczyk","year":"2002","unstructured":"Graczyk TK, Bosco-Nizeyi J, Ssebide B, Thompson RC, Read C, Cranfield MR: Anthropozoonotic Giardia duodenalis genotype (assemblage) A infections in habitats of free-ranging human-habituated gorillas, Uganda. J Parasitol. 2002, 88: 905-909.","journal-title":"J Parasitol"},{"key":"451_CR35","doi-asserted-by":"publisher","first-page":"857","DOI":"10.1016\/j.envres.2009.07.007","volume":"109","author":"YA Lim","year":"2009","unstructured":"Lim YA, Lai MM, Mahdy MAK, Mat Naim HR, Smith HV: Molecular detection of Giardia contamination in water bodies in a zoo. Environ Res. 2009, 109: 857-859.","journal-title":"Environ Res"},{"key":"451_CR36","doi-asserted-by":"publisher","first-page":"283","DOI":"10.1016\/j.vetpar.2005.05.061","volume":"133","author":"T Itagaki","year":"2005","unstructured":"Itagaki T, Kinoshita S, Aoki M, Itoh N, Saeki H, Sato N, Uetsuki J, Izumiyama S, Yagita K, Endo T: Genotyping of Giardia intestinalis from domestic and wild animals in Japan using glutamete dehydrogenase gene sequencing. Vet Parasitol. 2005, 133: 283-287.","journal-title":"Vet Parasitol"},{"key":"451_CR37","doi-asserted-by":"publisher","first-page":"410","DOI":"10.1016\/j.pt.2009.06.002","volume":"25","author":"G Ortega-Pierres","year":"2009","unstructured":"Ortega-Pierres G, Smith HV, Cacci\u00f2 SM, Thompson RC: New tools provide further insights into Giardia and Cryptosporidium biology. Trends Parasitol. 2009, 25: 410-416.","journal-title":"Trends Parasitol"}],"container-title":["Parasites &amp; Vectors"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/1756-3305-4-199.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,9,1]],"date-time":"2021-09-01T13:11:03Z","timestamp":1630501863000},"score":1,"resource":{"primary":{"URL":"https:\/\/parasitesandvectors.biomedcentral.com\/articles\/10.1186\/1756-3305-4-199"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2011,10,12]]},"references-count":37,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2011,12]]}},"alternative-id":["451"],"URL":"https:\/\/doi.org\/10.1186\/1756-3305-4-199","relation":{},"ISSN":["1756-3305"],"issn-type":[{"value":"1756-3305","type":"electronic"}],"subject":[],"published":{"date-parts":[[2011,10,12]]},"assertion":[{"value":"15 June 2011","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"12 October 2011","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"12 October 2011","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}}],"article-number":"199"}}